Advertisement

Biological Invasions

, Volume 19, Issue 1, pp 425–441 | Cite as

Aggressive interactions between two invasive species: the round goby (Neogobius melanostomus) and the spinycheek crayfish (Orconectes limosus)

  • Kathleen Church
  • Josephine C. Iacarella
  • Anthony RicciardiEmail author
Original Paper

Abstract

The invasion success of introduced species may be limited by competitive interactions with phylogenetically unrelated invaders. The round goby (Neogobius melanostomus) and spinycheek crayfish (Orconectes limosus) are invasive benthic predators that occupy and defend similar cryptic microhabitats, and thus may compete for shelter. The round goby expanded throughout the North American Great Lakes within 8 years of introduction, whereas another 6 years passed before it had spread through the upper St. Lawrence River. Here, we explore the premise that dense established populations of the invasive spinycheek crayfish slowed round goby colonization of the St. Lawrence River. We performed a series of videotaped laboratory experiments to determine if round gobies suffer from aggressive attacks or alter their behaviour (e.g. use of shelter and movement) in the presence of spinycheek crayfish. We also assessed the prolonged effects of food and shelter competition by comparing changes in the submerged mass of juvenile round gobies and spinycheek crayfish in conspecific and heterospecific pairs. Contrary to our predictions, round gobies more frequently initiated aggressive encounters with spinycheek crayfish, whereas the crayfish were more likely to flee or be evicted from their shelters. Furthermore, round gobies gained more body mass than spinycheek crayfish, regardless of conspecific or heterospecific pairing. Rather than impeding round goby colonization, spinycheek crayfish appear more likely to suffer energetic costs and an increased exposure to predation in the presence of round gobies.

Keywords

Aggression Agonistic behaviour Interspecific competition Crustacean Freshwater fish Invasive species 

Notes

Acknowledgments

The authors are grateful to N. Bayani, L. Jones, A. Kestrup, and R. Kipp for assistance in the field, to A. Hassan and R. Marrotte for assistance in the lab, to G. Larocque for assistance with the statistical methods, and to P. Chuard and J. Grant for helpful comments on an earlier version of the manuscript. This research was funded by the Canadian Aquatic Invasive Species Network (CAISN).

References

  1. Astorga N, Afonso MJ, Zamorano MJ, Montero D, Oliva V, Fernandez H, Izquierdo MS (2005) Evaluation of visible implant elastomer tags for tagging juvenile gilthead seabream (Sparus auratus L.); effects on growth, mortality, handling time and tag loss. Aquacult Res 36:733–738CrossRefGoogle Scholar
  2. Balshine S, Verma A, Chant V, Theysmeyer T (2005) Competitive interactions between round gobies and logperch. J Great Lakes Res 31:68–77CrossRefGoogle Scholar
  3. Bartoń K (2015) MuMIn: multi-model inference. R package version 1.15.1. http://CRAN.R-project.org/package=MuMIn
  4. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1-7. http://CRAN.R-project.org/package=lme4
  5. Bauer CR, Bobeldyk AM, Lamberti GA (2007) Predicting habitat use and trophic interactions of Eurasian ruffe, round gobies, and zebra mussels in nearshore areas of the Great Lakes. Biol Invas 9:667–678CrossRefGoogle Scholar
  6. Bergman DA, Moore PA (2003) Field observations of intraspecific antagonistic behaviour of two crayfish species, Orconectes rusticus and Orconectes virilis, in different habitats. Biol Bull 205:26–35CrossRefPubMedGoogle Scholar
  7. Bergstrom MA, Mensinger AF (2009) Interspecific resurce competition between the invasive round goby and three native species: logperch, slimy sculpin, and spoonhead sculpin. Trans Am Fish Soc 138:1009–1017CrossRefGoogle Scholar
  8. Blight O, Provost E, Renucci M, Tirard A, Orgeas J (2010) A native ant armed to limit the spread of the Argentine ant. Biol Invas 12:3785–3793CrossRefGoogle Scholar
  9. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135CrossRefPubMedGoogle Scholar
  10. Brandner J, Cerwenka AF, Schliewen UK, Geist J (2013) Bigger is better: characteristics of round gobies forming an invasion front in the Danube River. PLoS One 8:e73036CrossRefPubMedPubMedCentralGoogle Scholar
  11. Brownscombe JW, Fox MG (2012) Range expansion dynamics of the invasive round goby (Neogobius melanostomus) in a river system. Aquat Ecol 46:175–189CrossRefGoogle Scholar
  12. Bubb DH, O’Malley OJ, Gooderham AC, Lucas MC (2009) Relative impacts of native and non-native crayfish on shelter use by an indigenous benthic fish. Aquat Conserv 19:448–455CrossRefGoogle Scholar
  13. Butler MJ, Stein RA (1985) An analysis of the mechanisms governing species replacements in crayfish. Oecologica 66:168–177CrossRefGoogle Scholar
  14. Capelli GM, Munjal BL (1982) Aggressive interactions and resource competition in relation to species displacement among crayfish of the genus Orconectes. J Crustacean Biol 2:486–492CrossRefGoogle Scholar
  15. Carpenter J (2005) Competition for food between an introduced crayfish and two fishes endemic to the Colorado River basin. Environ Biol Fish 72:335–342CrossRefGoogle Scholar
  16. Charlebois, PM, Marsden, JE, Goettel, RG, Wolfe, RK, Jude, DJ, Rudnicka, S (1997) The round goby, Neogobius melanostomus (Pallus), a review of European and North American literature. Illinois-Indiana Sea Grant Program and Illinois Natural History Survey. INHS Special publication No. 20Google Scholar
  17. Christensen RHB (2015) ordinal—regression models for ordinal data. R package version 2015.1-21. http://www.cran.r-project.org/package=ordinal
  18. Chucholl C, Stich HB, Maier G (2008) Aggressive interactions and competition for shelter between a recently introduced and an established invasive crayfish: Orconectes immunis versus O. limosus. Fund Appl Limnol 172:27–36CrossRefGoogle Scholar
  19. Cooper MJ, Ruetz CR III, Uzarski DG, Burton TM (2007) Distribution of round gobies in coastal areas of Lake Michigan: Are wetlands resistant to invasion? J Great Lakes Res 33:303–313CrossRefGoogle Scholar
  20. Corkum LD, MacInnis AJ, Wickett RG (1998) Reproductive habits of round gobies. Great Lakes Res Rev 3:13–20Google Scholar
  21. Dietrich JP, Morrison BJ, Hoyle JA (2006) Alternative ecological pathways in the eastern Lake Ontario food web—round goby in the diet of lake trout. J Great Lakes Res 32:395–400CrossRefGoogle Scholar
  22. Dubé J, Desroches J-F (2007) Les écrevisses du Québec. Ministère des ressources naturelles et de la faune, Direction de l’aménagement de la faune de l’Estrie, de Montréal et de la Montérégie, LongueuilGoogle Scholar
  23. Dubs DOL, Corkum LD (1996) Behavioural interactions between round gobies (Neogobius melanostomus) and mottled sculpins (Cottus bairdi). J Great Lakes Res 22:838–844CrossRefGoogle Scholar
  24. Duckworth RA, Badyaev AV (2007) Coupling of dispersal and aggression facilitates the rapid range expansion of a passerine bird. Proc Natl Acad Sci USA 104(38):15017–15022CrossRefPubMedPubMedCentralGoogle Scholar
  25. Eros T, Sevcsik A, Toth B (2005) Abundance and night-time habitat use patterns of Ponto-Caspian gobiid species (Pisces, Gobiidae) in the littoral zone of the River Danube, Hungary. J Appl Ichthyol 21:350–357CrossRefGoogle Scholar
  26. Figler MH, Twum M, Finkelstein JE, Peeke HVS (1995) Maternal aggression in red swamp crayfish (Procambarus clarkii, Girard): the relation between reproductive status and outcome of aggressive encounters with male and female conspecifics. Behaviour 132:107–125CrossRefGoogle Scholar
  27. Figler MH, Cheverton HM, Blank GS (1999) Shelter competition in juvenile red swamp crayfish (Procambarus clarkii): the influences of sex differences, relative size, and prior residence. Aquaculture 178:63–75CrossRefGoogle Scholar
  28. Gherardi F, Cioni A (2004) Agonism and interference competition in freshwater decapods. Behaviour 141:1297–1324CrossRefGoogle Scholar
  29. Gherardi F, Daniels WH (2004) Agonism and shelter competition between invasive and indigenous crayfish species. Can J Zool 82:1923–1932CrossRefGoogle Scholar
  30. Griffen BD, Guy T, Buck JC (2008) Inhibition between invasives: a newly introduced predator moderates the impacts of a previously established invasive predator. J Anim Ecol 77:32–40CrossRefPubMedGoogle Scholar
  31. Griffiths SW, Collen P, Armstrong JD (2004) Competition for shelter among over-wintering signal crayfish and juvenile Atlantic salmon. J Fish Biol 65:436–447CrossRefGoogle Scholar
  32. Gutowsky LFG, Fox MG (2011) Occupation, body size and sex ratio of round goby (Neogobius melanostomus) in established and newly invaded areas of an Ontario river. Hydrobiologia 671:27–37CrossRefGoogle Scholar
  33. Haertel-Borer SS, Zak D, Eckmann R, Baade U, Holker F (2005) Population density of the crayfish, Orconectes limosus, in relation to fish and macroinvertebrate densities in a small mesotrophic lake—implications for the lake’s food web. Int Rev Hydrobiol 90:523–533CrossRefGoogle Scholar
  34. Hickey MBC, Fowlie AR (2005) First occurrence of the Round Goby, Neogobius melanostomus, in the St. Lawrence River at Cornwall, Ontario. Can Field Nat 119:582–583Google Scholar
  35. Hill AM, Lodge DM (1999) Replacement of resident crayfishes by an exotic crayfish: the roles of competition and predation. Ecol Appl 9:678–690CrossRefGoogle Scholar
  36. Hirsch PE, Fischer P (2008) Interactions between native juvenile burbot (Lota lota) and the invasive spinycheek crayfish (Orconectes limosus) in a large European lake. Can J Fish Aquat Sci 65:2636–2643CrossRefGoogle Scholar
  37. Holdich D, Black J (2007) The spiny-cheek crayfish, Orconectes limosus (Rafinesque, 1817) [Crustacea: Decapoda: Cambaridae], digs into the UK. Aquat Invas 2:1–16CrossRefGoogle Scholar
  38. Holway DA, Suarez AV (1999) Animal behaviour: an essential component of invasion biology. Trends Ecol Evol 14:328–330CrossRefPubMedGoogle Scholar
  39. Hudina S, Galić N, Roessink I, Hock K (2011) Competitive interactions between co-occurring invaders: identifying asymmetries between two invasive crayfish species. Biol Invasions 13:1791–1803CrossRefGoogle Scholar
  40. Hudina S, Hock K, Žganec K (2014) The role of aggression in range expansion and biological invasions. Curr Zool 60:401–409CrossRefGoogle Scholar
  41. James J, Thomas JR, Ellis A, Young KA, England J, Cable J (2016) Over-invasion in a freshwater ecosystem: newly introduced virile crayfish (Orconectes virilis) outcompete established invasive signal crayfish (Pacifastacus leniusculus). Mar Freshw Behav Physiol 49(1):9–18CrossRefGoogle Scholar
  42. Janssen J, Jude DJ (2001) Recruitment failure of mottled sculpin Cottus bairdi in Calumet Harbor, southern Lake Michigan, induced by the newly introduced round goby Neogobius melanostomus. J Great Lakes Res 27:319–328CrossRefGoogle Scholar
  43. Johnson PTJ, Olden JD, Solomon CT, Zanden MJV (2009) Interactions among invaders: community and ecosystem effects of multiple invasive species in an experimental aquatic system. Oecologia 159:161–170CrossRefPubMedGoogle Scholar
  44. Jude DJ (2001) Round and tubenose gobies: 10 years with the latest Great Lakes phantom menace. Dreissena 11:1–14Google Scholar
  45. Karanavanich C, Atema J (1998) Individual recognition and memory in lobster dominance. Anim Behav 56:1553–1560CrossRefGoogle Scholar
  46. Karlson AML, Almqvist G, Skora KE, Appelberg M (2007) Indications of competition between non-indigenous round goby and native flounder in the Baltic Sea. ICES J Mar Sci 64:1–8CrossRefGoogle Scholar
  47. Kipp R, Ricciardi A (2012) Impacts of the Eurasian round goby (Neogobius melanostomus) on benthic communities in the upper St. Lawrence River. Can J Fish Aquat Sci 69:469–486CrossRefGoogle Scholar
  48. Kipp R, Hébert I, Lacharité M, Ricciardi A (2012) Impacts of predation by the Eurasion round goby (Neogobius melanostomus) on molluscs in the upper St. Lawrence River. J Great Lakes Res 38:78–89CrossRefGoogle Scholar
  49. Klocker CA, Strayer DL (2004) Interactions among an invasive crayfish (Orconectes rusticus), a native crayfish (Orconectes limosus), and native bivalves (Sphaeriidae and Unionidae). Northeast Nat 11:167–178CrossRefGoogle Scholar
  50. Kobak J, Rachalewski M, Bacela-Spychalska K (2016) Conquerors or exiles? Impact of interference competition among invasive Ponto-Caspian gammarideans on their dispersal rates. Biol Invas 18(7):1953–1965CrossRefGoogle Scholar
  51. Kozák P, Buřič M, Policar T, Hamáčková J, Lepičová A (2007) The effect of inter- and intra-specific competition on survival and growth rate of native juvenile noble crayfish Astacus astacus and alien spiny-cheek crayfish Orconectes limosus. Hydrobiologica 590:85–94CrossRefGoogle Scholar
  52. Lenth RV (2016) Least-squares means: the R Package lsmeans. J Stat Softw 69:1–33CrossRefGoogle Scholar
  53. Light T (2005) Behavioural effects of invaders: alien crayfish and native sculpin in a California stream. Biol Invas 7:353–367CrossRefGoogle Scholar
  54. MacInnis AJ, Corkum LD (2000) Fecundity and reproductive season of the round goby Neogobius melanostomus in the upper Detroit River. Trans Am Fish Soc 129:136–144CrossRefGoogle Scholar
  55. Malone JC, Forrester GE, Steele MA (1999) Effects of subcutaneous microtags on the growth, survival, and vulnerability to predation of small reef fishes. J Exp Mar Biol Ecol 237:243–253CrossRefGoogle Scholar
  56. McMahon A, Patullo BW, Macmillan DL (2005) Exploration in a T-maze by the crayfish Cherax destructor suggests bilateral comparison of antennal tactile information. Biol Bull 208:183–188CrossRefPubMedGoogle Scholar
  57. Momot WT, Gowing H, Jones PD (1978) Dynamics of crayfish and their role in ecosystems. Am Midl Nat 99:10–35CrossRefGoogle Scholar
  58. Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci USA 98(10):5446–5451CrossRefPubMedPubMedCentralGoogle Scholar
  59. Nakata K, Goshima S (2003) Competition for shelter of preferred sizes between the native crayfish species Cambaroides japonicus and the alien crayfish species Cambaroides japonicus and the alien crayfish species Pacifastacus leniusculus in Japan in relation to prior residence, sex difference and body size. J Crustacean Biol 23:897–907CrossRefGoogle Scholar
  60. Olsen EM, Vollestad LA (2001) An evaluation of visible implant elastomer for marking age-0 brown trout. North Am J Fish Manage 21:967–970CrossRefGoogle Scholar
  61. Parkyn SM, Collier KJ, Hicks BJ (2002) Growth and population dynamics of crayfish Paranephrops planifrons in streams within native forest and pastoral land uses. N Zeal J Mar Fresh 36:847–861CrossRefGoogle Scholar
  62. Patullo BW, Macmillan DL (2006) Corners and bubble wrap: the structure and texture of surfaces influence crayfish exploratory behaviour. J Exp Biol 209:567–575CrossRefPubMedGoogle Scholar
  63. Peeke HVS, Sippel J, Figler MH (1995) Prior residence effects in shelter defense in adult signal crayfish (Pacifastacus leniusculus) results in same- and mixed-sex dyads. Crustaceana 68:873–881CrossRefGoogle Scholar
  64. Percival DT, Moore PT (2010) Shelter size influences self-assessment of size in crayfish, Orconectes rusticus: consequences for agonistic fights. Behaviour 147:103–119CrossRefGoogle Scholar
  65. Phillips EC, Washek ME, Hertel AW, Niebel BM (2003) The round goby (Neogobius melanostomus) in Pennsylvania tributary streams of Lake Erie. J Great Lakes Res 29:34–40CrossRefGoogle Scholar
  66. Pintor LM, Sih A, Bauer ML (2008) Differences in aggression, activity and boldness between native and introduced populations of an invasive crayfish. Oikos 117:1629–1636CrossRefGoogle Scholar
  67. Piscart C, Roussel JM, Dick JTA, Grosbois G, Marmonier P (2011) Effects of coexistence on habitat use and trophic ecology of interacting native and invasive amphipods. Fresh Biol 56:325–334CrossRefGoogle Scholar
  68. Preston DL, Henderson JS, Johnson PTJ (2012) Community ecology of invasions: direct and indirect effects of multiple invasive species on aquatic communities. Ecology 93(6):1254–1261CrossRefPubMedGoogle Scholar
  69. Ray WJ, Corkum LD (1997) Predation of zebra mussels by round gobies, Neogobius melanostomus. Environ Biol Fish 50:267–273CrossRefGoogle Scholar
  70. Ray WJ, Corkum LD (2001) Habitat and site affinity of the round goby. J Great Lakes Res 27:329–334CrossRefGoogle Scholar
  71. Ricciardi A, Whoriskey FG, Rasmussen JB (1997) The role of the zebra mussel (Dreissena polymorpha) in structuring macroinvertebrate communities on hard substrata. Can J Fish Aquat Sci 54:2596–2608CrossRefGoogle Scholar
  72. Savino JF, Riley SC, Holuszko MJ (2007) Activity, aggression and habitat use of ruffe (Gymnocephalus cernuus) and round goby (Apollonia menanostoma) under laboratory conditions. J Great Lakes Res 33:326–334CrossRefGoogle Scholar
  73. Söderbäck B (1991) Interspecific dominance relationship and aggressive interactions in the freshwater crayfish Astacus astacus (L.) and Pacifastacus leniusculus (Dana). Can J Zool 69:1321–1325CrossRefGoogle Scholar
  74. Stammler KL, Corkum LD (2005) Assessment of fish size on shelter choice and intraspecific interactions by round gobies Neogobius melanostomus. Environ Biol Fish 73:117–123CrossRefGoogle Scholar
  75. Steele C, Skinner C, Steele C, Alberstadt P, Mathewson C (1999) Organization of chemically activated food search behavior in Procambarus clarkii Girard and Orconectes rusticus Girard crayfishes. Biol Bull 196:295–302CrossRefGoogle Scholar
  76. Stein RA, Magnuson JJ (1976) Behavioural response of crayfish to a fish predator. Ecology 57(4):751–761CrossRefGoogle Scholar
  77. Thompson KA, Hill JE, Nico LG (2012) Eastern mosquitofish resists invasion by nonindigenous poeciliids through agonistic behaviors. Biol Invas 14:1515–1529CrossRefGoogle Scholar
  78. Tricarico E, Gherardi F (2010) Past ownership makes crayfish more aggressive. Behav Ecol Sociobiol 64:575–581CrossRefGoogle Scholar
  79. Usio N, Konishi M, Nakano S (2001) Species displacement between an introduced and a ‘vulnerable’ crayfish: the role of aggressive interactions and shelter competition. Biol Invas 3:179–185CrossRefGoogle Scholar
  80. Vorburger C, Ribi G (1999) Aggression and competition for shelter between a native and an introduced crayfish in Europe. Fresh Biol 42:111–119CrossRefGoogle Scholar
  81. Walsh MG, Dittman DE, O’Gorman R (2007) Occurrence and food habits of the round goby in the profundal zone of Southwestern Lake Ontario. J Great Lakes Res 33:83–92CrossRefGoogle Scholar
  82. Zheng J, Mao R, Zhang R (2008) Competitive interactions between the yellow crazy ant and the red imported fire ant (Hymenoptera: Formicidae). J Entomol Sci 43(3):331–336Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of BiologyConcordia UniversityMontrealCanada
  2. 2.Department of BiologyUniversity of VictoriaVictoriaCanada
  3. 3.Redpath MuseumMcGill UniversityMontrealCanada

Personalised recommendations